Temporally distinct PD-L1 expression by tumor and host cells contributes to immune escape

Cancer Immunology Research

Volumn 5, Issue 2, 2017, Pages 106-117

  Noguchi, Takuro ^a   Ward, Jeffrey P ^a   Gubin, Matthew M ^a   Arthur, Cora D ^a   Lee, Sang Hun ^a   Hundal, Jasreet ^a   Selby, Mark J ^b   Graziano, Robert F ^c   Mardis, Elaine R ^a   Korman, Alan J ^b   Schreiber, Robert D ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Bristol Myers Squibb   (United States)

^c BRISTOL MYERS SQUIBB   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 METHYLCHOLANTHRENE; GAMMA INTERFERON; PROGRAMMED DEATH 1 LIGAND 1; RAG2 PROTEIN; SPECTRIN; SPECTRIN BETA2; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; COLORECTAL CANCER CELL LINE; CONTROLLED STUDY; CRISPR CAS SYSTEM; DRUG ANTIGENICITY; FEMALE; GAIN OF FUNCTION MUTATION; GENE EDITING; GENE OVEREXPRESSION; GLYCOSYLATION; HOST CELL; IMMUNOCOMPETENT CELL; IN VIVO STUDY; LOSS OF FUNCTION MUTATION; MALE; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; POINT MUTATION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SARCOMA; SARCOMA CELL; SOMATIC MUTATION; STOP CODON; TUMOR ASSOCIATED LEUKOCYTE; TUMOR CELL; TUMOR ESCAPE; TUMOR IMMUNOGENICITY; TUMOR MICROENVIRONMENT; TUMOR REJECTION; UPREGULATION; ANIMAL; CELL PROLIFERATION; DISEASE MODEL; GENE; GENE EXPRESSION; GENE INACTIVATION; GENETICS; HUMAN; IMMUNOLOGY; MUTATION; NEOPLASM; PATHOLOGY; TUMOR CELL LINE; TUMOR VOLUME;

ANIMALS; B7-H1 ANTIGEN; CELL LINE, TUMOR; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION; GENE KNOCKOUT TECHNIQUES; GENES, MHC CLASS I; HUMANS; MALE; MICE; MUTATION; NEOPLASMS; SARCOMA; TUMOR BURDEN; TUMOR ESCAPE; TUMOR MICROENVIRONMENT;

EID: 85016130258     PISSN: 23266066     EISSN: 23266074     Source Type: Journal    
DOI: 10.1158/2326-6066.CIR-16-0391     Document Type: Article

References (50)

1. Dong H, Strome SE, Salomao DR, Tamura H, Hirano F, Flies DB, et al. Tumor-associated B7-H1 promotes T-cell apoptosis: A potential mechanism of immune evasion. Nat Med 2002;8:793-800.
2. Iwai Y, Ishida M, Tanaka Y, Okazaki T, Honjo T, Minato N. Involvement of PD-L1 on tumor cells in the escape from host immune system and tumor immunotherapy by PD-L1 blockade. Proc Natl Acad Sci 2002;99:12293-7.
3. Borghaei H, Paz-Ares L, Horn L, Spigel DR, Steins M, Ready NE, et al. Nivolumab versus docetaxel in advanced nonsquamous non-small-cell lung cancer. N Engl J Med 2015;373:1627-39.
4. Garon EB, Rizvi NA, Hui R, Leighl N, Balmanoukian AS, Eder JP, et al. Pembrolizumab for the treatment of non-small-cell lung cancer. N Engl J Med 2015;372:2018-28.
5. Rittmeyer A, Barlesi F, Waterkamp D, Park K, Ciardiello F, Pawel von J, et al. Atezolizumab versus docetaxel in patients with previously treated nonsmall-cell lung cancer (OAK): A phase 3, open-label, multicentre randomised controlled trial. Lancet 2016 Dec 12. [Epub ahead of print].
6. Keir ME, Butte MJ, Freeman GJ, Sharpe AH. PD-1 and its ligands in tolerance and immunity. Annu Rev Immunol 2008;26: 677-704.
7. Latchman YE, Liang SC, Wu Y, Chernova T, Sobel RA, Klemm M, et al. PDL1-deficientmice show that PD-L1 on T cells, antigen-presenting cells, and host tissues negatively regulates T cells. Proc Natl Acad Sci 2004;101: 10691-6.
8. Keir ME, Liang SC, Guleria I, Latchman YE, Qipo A, Albacker LA, et al. Tissue expression of PD-L1 mediates peripheral T cell tolerance. J Exp Med 2006;203:883-95.
9. Topalian SL, Drake CG, Pardoll DM. Immune checkpoint blockade: A common denominator approach to cancer therapy. Cancer Cell 2015; 27:450-61.
10. Weber JS, D'Angelo SP, Minor D, Hodi FS, Gutzmer R, Neyns B, et al. Nivolumab versus chemotherapy in patients with advanced melanoma who progressed after anti-CTLA-4 treatment (CheckMate 037): a randomised, controlled, open-label, phase 3 trial. Lancet Oncol 2015; 16:375-84.
11. Reck M, Rodríguez-Abreu D, Robinson AG, Hui R, Cso szi T, Fülöp A, et al. Pembrolizumab versus chemotherapy for PD-L1-positive non-small-cell lung cancer. N Engl J Med 2016;375:1823-33.
12. Robert C, Long GV, Brady B, Dutriaux C, Maio M, Mortier L, et al. Nivolumab in previously untreated melanoma without BRAF mutation. N Engl J Med 2015;372:320-30.
13. Ferris RL, Blumenschein G, Fayette J, Guigay J, Colevas AD, Licitra L, et al. Nivolumab for recurrent squamous-cell carcinoma of the head and neck. N Engl J Med 2016;375:1856-67.
14. Brahmer J, Reckamp KL, Baas P, Crinò L, Eberhardt WEE, Poddubskaya E, et al. Nivolumab versus docetaxel in advanced squamous-cell non-smallcell lung cancer. N Engl J Med 2015;373:123-35.
15. Chow LQM, Haddad R, Gupta S, Mahipal A, Mehra R, Tahara M, et al. Antitumor activity of pembrolizumab in biomarker-unselected patients with recurrent and/or metastatic head and neck squamous cell carcinoma: Results from the phase Ib KEYNOTE-012 expansion cohort. J Clin Oncol. 2016:JCO681478.
16. Nghiem PT, Bhatia S, Lipson EJ, Kudchadkar RR, Miller NJ, Annamalai L, et al. PD-1 blockade with pembrolizumab in advanced Merkel-cell carcinoma. N Engl J Med 2016;374:2542-52.
17. Rosenberg JE, Hoffman-Censits J, Powles T, van der Heijden MS, Balar AV, Necchi A, et al. Atezolizumab in patients with locally advanced and metastatic urothelial carcinoma who have progressed following treatment with platinum-based chemotherapy: A single-arm, multicentre, phase 2 trial. Lancet 2016;387:1909-20.
18. Balar AV, Galsky MD, Rosenberg JE, Powles T, Petrylak DP, Bellmunt J, et al. Atezolizumab as first-line treatment in cisplatin-ineligible patients with locally advanced and metastatic urothelial carcinoma: A single-arm, multicentre, phase 2 trial. Lancet 2016;389:67-76.
19. Curiel TJ, Wei S, Dong H, Alvarez X, Cheng P, Mottram P, et al. Blockade of B7-H1 improves myeloid dendritic cell-mediated antitumor immunity. Nat Med 2003;9:562-7.
20. Chen L, Gibbons DL, Goswami S, Cortez MA, Ahn Y-H, Byers LA, et al. Metastasis is regulated via microRNA-200/ZEB1 axis control of tumour cell PD-L1 expression and intratumoral immunosuppression. Nat Commun 2014;5:5241-12.
21. Victor CT-S, Rech AJ, Maity A, Rengan R, Pauken KE, Stelekati E, et al. Radiation and dual checkpoint blockade activate non-redundant immune mechanisms in cancer. Nature 2015;520:373-7.
22. Kataoka K, Shiraishi Y, Takeda Y, Sakata S, Matsumoto M, Nagano S, et al. Aberrant PD-L1 expression through 3′-UTR disruption in multiple cancers. Nature 2016;534:402-6.
23. Green MR, Monti S, Rodig SJ, Juszczynski P, Currie T, O'Donnell E, et al. Integrative analysis reveals selective 9p24.1 amplification, increased PD-1 ligand expression, and further induction via JAK2 in nodular sclerosing Hodgkin lymphoma and primary mediastinal large B-cell lymphoma. Blood 2010;116:3268-77.
24. Fehrenbacher L, Spira A, Ballinger M, Kowanetz M, Vansteenkiste J, Mazieres J, et al. Atezolizumab versus docetaxel for patients with previously treated non-small-cell lung cancer (POPLAR): A multicentre, open-label, phase 2 randomised controlled trial. Lancet 2016;387: 1837-46.
25. Bellmunt J, Mullane SA, Werner L, Fay AP, Callea M, Leow JJ, et al. Association of PD-L1 expression on tumor-infiltrating mononuclear cells and overall survival in patients with urothelial carcinoma. Ann Oncol 2015;26:812-7.
26. Hatogai K, Kitano S, Fujii S, Kojima T, Daiko H, Nomura S, et al. Comprehensive immunohistochemical analysis of tumor microenvironment immune status in esophageal squamous cell carcinoma. Oncotarget 2016;7:47252-64.
27. Shankaran V, Ikeda H, Bruce AT, White JM, Swanson PE, Old LJ, et al. IFNgamma and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature 2001;410: 1107-11.
28. Matsushita H, Vesely MD, Koboldt DC, Rickert CG, Uppaluri R, Magrini VJ, et al. Cancer exome analysis reveals a T-cell-dependent mechanism of cancer immunoediting. Nature 2012;482:400-4.
29. Gubin MM, Zhang X, Schuster H, Caron E, Ward JP, Noguchi T, et al. Checkpoint blockade cancer immunotherapy targets tumour-specific mutant antigens. Nature 2014;515:577-81.
30. Hundal J, Carreno BM, Petti AA, Linette GP, Griffith OL, Mardis ER, et al. pVAC-Seq: A genome-guided in silico approach to identifying tumor neoantigens. Genome Med 2016;8:337-11.
31. Yu Y-RA, O'Koren EG, Hotten DF, Kan MJ, Kopin D, Nelson ER, et al. A protocol for the comprehensive flowcytometric analysis ofimmune cells in normal and inflamed murine non-lymphoid tissues. PLoS ONE 2016;11: e0150606.
32. Dahan R, Sega E, Engelhardt J, Selby M, Korman AJ, Ravetch JV. FcgRs modulate the anti-tumor activity of antibodies targeting the PD-1/PD-L1 axis. Cancer Cell 2015;28:285-95.
33. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The sequence alignment/map format and SAMtools. Bioinformatics 2009;25: 2078-9.
34. Li H. A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics 2011;27:2987-93.
35. Larson DE, Harris CC, Chen K, Koboldt DC, Abbott TE, Dooling DJ, et al. SomaticSniper: Identification of somatic point mutations in whole genome sequencing data. Bioinformatics 2012;28:311-7.
36. Koboldt DC, Chen K, Wylie T, Larson DE, McLellan MD, Mardis ER, et al. VarScan: Variant detection in massively parallel sequencing of individual and pooled samples. Bioinformatics 2009;25:2283-5.
37. Koboldt DC, Zhang Q, Larson DE, Shen D, McLellan MD, Lin L, et al. VarScan 2: Somatic mutation and copy number alteration discovery in cancer by exome sequencing. Genome Res 2012;22:568-76.
38. Schreiber RD, Old LJ, Smyth MJ. Cancer immunoediting: Integrating immunity's roles in cancer suppression and promotion. Science 2011; 331:1565-70.
39. Andreatta M, Nielsen M. Gapped sequence alignment using artificial neural networks: Application to the MHC class I system. Bioinformatics 2016; 32:511-7.
40. Latchman Y, Wood CR, Chernova T, Chaudhary D, Borde M, Chernova I, et al. PD-L2 is a second ligand for PD-1 and inhibits T cell activation. Nat Immunol 2001;2:261-8.
41. Mathios D, Ruzevick J, Jackson CM, Xu H, Shah S, Taube JM, et al. PD-1, PDL1, PD-L2 expression in the chordoma microenvironment. J Neurooncol 2014;121:251-9.
42. Rodig N, Ryan T, Allen JA, Pang H, Grabie N, Chernova T, et al. Endothelial expression of PD-L1 and PD-L2 down-regulates CD8+T cell activation and cytolysis. Eur J Immunol 2003;33:3117-26.
43. Hildner K, Edelson BT, Purtha WE, Diamond M, Matsushita H, Kohyama M, et al. Batf3 deficiency reveals a critical role for CD8a+ dendritic cells in cytotoxic T cell immunity. Science 2008;322:1097-100.
44. Diamond MS, Kinder M, Matsushita H, Mashayekhi M, Dunn GP, Archambault JM, et al. Type I interferon is selectively required by dendritic cells for immune rejection of tumors. J Exp Med 2011;208:1989-2003.
45. Hobo W, Maas F, Adisty N, de Witte T, Schaap N, van der Voort R, et al. siRNA silencing of PD-L1 and PD-L2 on dendritic cells augments expansion and function of minor histocompatibility antigen-specific CD8+ T cells. Blood 2010;116:4501-11.
46. Kuang D-M, Zhao Q, Peng C, Xu J, Zhang J-P, Wu C, et al. Activated monocytes in peritumoral stroma of hepatocellular carcinoma foster immune privilege and disease progression through PD-L1. J Exp Med 2009;206:1327-37.
47. Ding Z-C, Lu X, Yu M, Lemos H, Huang L, Chandler P, et al. Immunosuppressive myeloid cells induced by chemotherapy attenuate antitumor CD4+ T-cell responses through the PD-1-PD-L1 axis. Cancer Res 2014;74: 3441-53.
48. Rizvi NA, Hellmann MD, Snyder A, Kvistborg P, Makarov V, Havel JJ, et al. Cancer immunology. Mutational landscape determines sensitivity to PD-1 blockade in non-small cell lung cancer. Science 2015;348:124-8.
49. Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer 2012;12:252-64.
50. Verdegaal EME, de Miranda NFCC, Visser M, Harryvan T, van Buuren MM, Andersen RS, et al. Neoantigen landscape dynamics during human melanoma-T cell interactions. Nature 2016;536:91-5.